Panic and the brainstem: Clues from neuroimaging studies

CNS and Neurological Disorders - Drug Targets

Volumn 13, Issue 6, 2014, Pages 1049-1056

  Perna, Giampaolo ^a,d,e   Guerriero, Giuseppe ^a   Brambilla, Paolo ^b,c   Caldirola, Daniela ^a  

^a Villa San Benedetto Hospital   (Italy)

^b UNIVERSITY OF UDINE   (Italy)

^c SCIENTIFIC INSTITUTE   (Italy)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Anxiety disorders; Brain imaging; Brainstem; Panic disorder; Provocation studies; Serotonergic receptors

Indexed keywords

CARBON DIOXIDE; PROTON; SEROTONIN RECEPTOR; SEROTONIN TRANSPORTER;

ARTERIAL CARBON DIOXIDE TENSION; ARTICLE; BLOOD FLOW; BRAIN FUNCTION; BRAIN STEM; CHEMORECEPTOR; GLUCOSE TRANSPORT; HEMOSTASIS; HUMAN; MAJOR DEPRESSION; MENTAL DISEASE; NEUROIMAGING; NONHUMAN; PANIC; RECEPTOR BINDING; RESPIRATION CONTROL; RESTING STATE NETWORK; SCORING SYSTEM; SEROTONINERGIC SYSTEM; STIMULUS; BIBLIOGRAPHIC DATABASE; CLASSIFICATION; METABOLISM; PATHOLOGY; RADIOASSAY; STATISTICS AND NUMERICAL DATA;

BRAIN STEM; DATABASES, BIBLIOGRAPHIC; HUMANS; NEUROIMAGING; PANIC DISORDER; RADIOLIGAND ASSAY; RECEPTORS, SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84924668437     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/1871527313666140612112923     Document Type: Article

References (98)

1. Gorman JM, Liebowitz MR, Fyer AJ, Stein J. A neuroanatomical hypothesis for panic disorder. Am J Psychiatry 1989; 146(2): 148-61.
2. Klein DF. False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch Gener Psychiatry 1993; 50(4): 306-17.
3. Perna G, Caldirola D, Bellodi L. Panic disorder: from respiration to the homeostatic brain. Acta Neuropsychiatr 2004; 16: 57-67.
4. Gorman JM, Kent JM, Sullivan GM, Coplan JD. Neuroanatomical hypothesis of panic disorder, revised. Am J Psychiatry 2000; 157(4): 493-505.
5. Ley R. Blood, breath, and fears: a hyperventilation theory of panic attacks and agoraphobia. Clin Psychol Rev 1985; 5: 271-85.
6. Perna G. Understanding anxiety disorders: the psychology and the psychopathology of defence mechanisms against threats. Rivista Psichiatria 2013; 48(1): 73-5.
7. Graeff FG, Del-Ben CM. Neurobiology of panic disorder: from animal models to brain neuroimaging. Neurosci Biobehav Rev 2008; 32(7): 1326-35.
8. Lim LW, Blokland A, Tan S, et al. Attenuation of fear-like response by escitalopram treatment after electrical stimulation of the midbrain dorsolateral periaqueductal gray. Exp Neurol 2010; 226(2): 293-300.
9. Johnson PL, Shekhar A. An animal model of panic vulnerability with chronic disinhibition of the dorsomedial/perifornical hypothalamus. Physiol Behav 2012; 107(5): 686-98.
10. Grassi M, Caldirola D, Vanni G, et al. Baseline respiratory parameters in panic disorder: a meta-analysis. J Affect Disord 2013; 146(2): 158-73.
11. Esquivel G, Schruers KR, Maddock RJ, Colasanti A, Griez EJ. Acids in the brain: a factor in panic? J Psychopharmacol 2010; 24(5): 639-47.
12. van Duinen MA, Schruers KR, Maes M, Griez EJ. CO2 challenge induced HPA axis activation in panic. Intl J Neuropsychopharmacol 2007; 10(6): 797-804.
13. Maddock RJ, Buonocore MH, Miller AR, et al. Abnormal activitydependent brain lactate and glutamate+glutamine responses in panic disorder. Biol Psychiatry 2013; 73(11): 1111-9.
14. Peskind ER, Jensen CF, Pascualy M, et al. Sodium lactate and hypertonic sodium chloride induce equivalent panic incidence, panic symptoms, and hypernatremia in panic disorder. Biol Psychiatry 1998; 44(10): 1007-16.
15. Abelson JL, Khan S, Liberzon I, Young EA. HPA axis activity in patients with panic disorder: review and synthesis of four studies. Depress Anxiety 2007; 24(1): 66-76.
16. Petrowski K, Wintermann GB, Schaarschmidt M, Bornstein SR, Kirschbaum C. Blunted salivary and plasma cortisol response in patients with panic disorder under psychosocial stress. Intl J Psychophysiol 2013; 88(1): 35-9.
17. Damasio AR. The Feeling of What Happens: Body and Emotion in the Making of Conscoiusness. USA: Mariner Books; 2000.
18. Dresler T, Guhn A, Tupak SV, et al. Revise the revised? New dimensions of the neuroanatomical hypothesis of panic disorder. J Neural Transm 2013; 120(1): 3-29.
19. Feldman JL, Del Negro CA, Gray PA. Understanding the rhythm of breathing: so near, yet so far. Annu Rev Physiol 2013; 75: 423-52.
20. Feldman JL, Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 2006; 7(3): 232-42.
21. Alheid GF, McCrimmon DR. The chemical neuroanatomy of breathing. Respir Physiol Neurobiol 2008; 164(1-2): 3-11.
22. Housley GD. Recent insights into the regulation of breathing. Auton Neurosci 2011; 164: 3-5.
23. Guyenet PG, Stornetta RL, Abbott SB, et al. Central CO2 chemoreception and integrated neural mechanisms of cardiovascular and respiratory control. J Appl Physiol 2010; 108(4): 995-1002.
24. Gargaglioni LH, Hartzler LK, Putnam RW. The locus coeruleus and central chemosensitivity. Respir Physiol Neurobiol 2010; 173(3): 264-73.
25. Moreira TS, Takakura AC, Damasceno RS, et al. Central chemoreceptors and neural mechanisms of cardiorespiratory control. Braz J Med Biol Res 2011; 44(9): 883-9.
26. Dick TE, Baekey DM, Paton JF, Lindsey BG, Morris KF. Cardiorespiratory coupling depends on the pons. Respir Physiol Neurobiol 2009; 168(1-2): 76-85.
27. Brandao ML, Zanoveli JM, Ruiz-Martinez RC, Oliveira LC, Landeira-Fernandez J. Different patterns of freezing behavior organized in the periaqueductal gray of rats: association with different types of anxiety. Behav Brain Res 2008; 188(1): 1-13.
28. Graeff FG. New perspective on the pathophysiology of panic: merging serotonin and opioids in the periaqueductal gray. Braz J Med Biol Res 2012; 45(4): 366-75.
29. Hilaire G, Voituron N, Menuet C, et al. The role of serotonin in respiratory function and dysfunction. Respir Physiol Neurobiol 2010; 174(1-2): 76-88.
30. Shao XM, Feldman JL. Acetylcholine modulates respiratory pattern: effects mediated by M3-like receptors in preBotzinger complex inspiratory neurons. J Neurophysiol 2000; 83(3): 1243-52.
31. Nattie E. CO2, brainstem chemoreceptors and breathing. Prog Neurobiol 1999; 59(4): 299-331.
32. Perna G, Guerriero G, Caldirola D. Emerging drugs for panic disorder. Expert Opin Emerg Drugs 2011; 16(4): 631-45.
33. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders DSM-III. Amer Psychiatric Publishers: Washington, DC 1980.
34. Association AP. Diagnostic and statistical manual of mental disorders DSM III-R. American Psychiatric Publishers: Washington DC 1987.
35. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders DSM-IV. Amer Psychiatric Publishers: Washington DC 1994.
36. Association AP. Diagnostic and Statistical Manual of Mental Disorders DSM-IV-TR Fourth Edition (Text Revision). Amer Psychiatric Publishers: Washington DC 2000.
37. Reiman EM, Raichle ME, Robins E, et al. Neuroanatomical correlates of a lactate-induced anxiety attack. Arch Gener Psychiatry 1989; 46(6): 493-500.
38. Wise RG, Ide K, Poulin MJ, Tracey I. Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 2004; 21(4): 1652-64.
39. Chang C, Glover GH. Relationship between respiration, end-tidal CO2, and BOLD signals in resting-state fMRI. Neuroimage 2009; 47: 1381-93.
40. Giardino ND, Friedman SD, Dager SR. Anxiety, respiration, and cerebral blood flow: implications for functional brain imaging. Compr Psychiatry 2007; 48(2): 103-12.
41. Dager SR. The vexing role of baseline: implications for neuroimaging studies of panic disorder. Intl J Psychophysiol 2010; 78(1): 20-6.
42. Boshuisen ML, Horst Ter G, Paans AMJ, Reinders AA, den Boer JA. rCBF differences between panic disorder patients and control subjects during anticipatory anxiety and rest. Biol Psychiatry 2002; 52: 126-35.
43. Kent JM, Coplan JD, Mawlawi O, et al. Prediction of panic response to a respiratory stimulant by reduced orbitofrontal cerebral blood flow in panic disorder. Am J Psychiatry 2005; 162(7): 1379-81.
44. Garakani A, Buchsbaum MS, Newmark RE, et al. The effect of doxapram on brain imaging in patients with panic disorder. Eur Neuropsychopharmacol 2007; 17(10): 672-86.
45. Goossens L, Leibold N, Peeters R, et al. Brainstem response to hypercapnia: a symptom provocation study into the pathophysiology of panic disorder. J Psychopharmacol 2014; 28: 449-56.
46. Gauthier CJ, Madjar C, Tancredi FB, Stefanovic B, Hoge RD. Elimination of visually evoked BOLD responses during carbogen inhalation: implications for calibrated MRI. Neuroimage 2011; 54(2): 1001-11.
47. Harvey AK, Pattinson KT, Brooks JC, et al. Brainstem functional magnetic resonance imaging: disentangling signal from physiological noise. J Magn Reson Imaging 2008; 28(6): 1337-44.
48. Windschberger C, Langenberger H, Sycha T, et al. On the origin of respiratory artifacts in bold-epi of the human brain. Magn Reson Imaging 2002; 20: 575-82.
49. Hayen A, Herigstad M, Kelly M, et al. The effects of altered intrathoracic pressure on resting cerebral blood flow and its response to visual stimulation. NeuroImage 2012; 66C: 479-88.
50. Sakai Y, Kumano H, Nishikawa M, et al. Cerebral glucose metabolism associated with a fear network in panic disorder. Neuroreport 2005; 16(9): 927-31.
51. Birn RM, Smith MA, Jones TB, Bandettini PA. The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. NeuroImage 2008; 40(2): 644-54.
52. Etkin A, Egner T, Peraza DM, Kandel ER, Hirsch J. Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 2006; 51(6): 871-82.
53. Chechko N, Wehrle R, Erhardt A, et al. Unstable prefrontal response to emotional conflict and activation of lower limbic structures and brainstem in remitted panic disorder. PloS One 2009; 4(5): e5537.
54. Tuescher O, Protopopescu X, Pan H, et al. Differential activity of subgenual cingulate and brainstem in panic disorder and PTSD. J Anxiety Disord 2011; 25(2): 251-7.
55. Bremner JD, Innis RB, White T, et al. SPECT I-123]iomazenil measurement of the benzodiazepine receptor in panic disorder. Biol Psychiatry 2000; 47(2): 96-106.
56. Neumeister A, Bain E, Nugent AC, et al. Reduced serotonin type 1A receptor binding in panic disorder. J Neurosci 2004; 24(3): 589-91.
57. Nash JR, Sargent PA, Rabiner EA, et al. Serotonin 5-HT1A receptor binding in people with panic disorder: positron emission tomography study. Br J Psychiatry 2008; 193(3): 229-34.
58. Maron E, Kuikka JT, Shlik J, et al. Reduced brain serotonin transporter binding in patients with panic disorder. Psychiatry Res 2004; 132(2): 173-81.
59. Maron E, Toru I, Hirvonen J, et al. Gender differences in brain serotonin transporter availability in panic disorder. J Psychopharmacol 2011; 25(7): 952-9.
60. Staley JK, Sanacora G, Tamagnan G, et al. Sex differences in diencephalon serotonin transporter availability in major depression. Biol Psychiatry 2006; 59(1): 40-7.
61. Jovanovic H, Lundberg J, Karlsson P, et al. Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. Neuroimage 2008; 39(3): 1408-19.
62. Nishizawa S, Benkelfat C, Young SN, et al. Differences between males and females in rates of serotonin synthesis in human brain. Proc Natl Acad Sci USA 1997; 94: 5308-13.
63. Praschak-Rieder N, Willeit M, Wilson AA, Houle S, Meyer JH. Seasonal variation in human brain serotonin transporter binding. Arch Gen Psychiatry 2008; 65(9): 1072-8.
64. Protopopescu X, Pan H, Tuescher O, et al. Increased brainstem volume in panic disorder: a voxel-based morphometric study. Neuroreport 2006; 17(4): 361-3.
65. Uchida RR, Del-Ben CM, Busatto GF, et al. Regional gray matter abnormalities in panic disorder: a voxel-based morphometry study. Psychiatry Res 2008; 163(1): 21-9.
66. Fujiwara A, Yoshida T, Otsuka T, et al. Midbrain volume increase in patients with panic disorder. Psychiatry Clin Neurosci 2011; 65(4): 365-73.
67. Sakai Y, Kumano H, Nishikawa M, et al. Changes in cerebral glucose utilization in patients with panic disorder treated with cognitive-behavioral therapy. Neuroimage 2006; 33(1): 218-26.
68. Lai CH, Wu YT. Duloxetine's modest short-term influences in subcortical structures of first episode drug-naive patients with major depressive disorder and panic disorder. Psychiatry Res 2011; 194(2): 157-62.
69. Lee HY, Tae WS, Yoon HK, et al. Demonstration of decreased gray matter concentration in the midbrain encompassing the dorsal raphe nucleus and the limbic subcortical regions in major depressive disorder: an optimized voxel-based morphometry study. J Affect Disord 2011; 133(1-2): 128-36.
70. Nicholls JG, Paton JF. Brainstem: neural networks vital for life. Phil Trans R Soc Lond Ser B Biol Sci 2009; 364(1529): 2447-51.
71. Mobbs D, Petrovic P, Marchant J, Hassabis D. When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science 2007; 317: 1079-83.
72. Del-Ben CM, Graeff FG. Panic Disorder: is the PAG involved? Neural Plast 2009; 2009: 108135.
73. Beissner F, Schumann A, Brunn F, Eisentrager D, Bar KJ. Advances in functional magnetic resonance imaging of the human brainstem. NeuroImage 2014; 86: 91-8.
74. Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med 2000; 44(1): 162-7.
75. Birn RM, Diamond JB, Smith MA, Bandettini PA. Separating respiratory-variation-related fluctuations from neuronal-activityrelated fluctuations in fMRI. Neuroimage 2006; 31(4): 1536-48.
76. Del Casale A, Serata D, Rapinesi C, et al. Structural neuroimaging in patients with panic disorder: findings and limitations of recent studies. Psychiatria Danubina 2013; 25(2): 108-14.
77. Feinstein JS, Buzza C, Hurlemann R, et al. Fear and panic in humans with bilateral amygdala damage. Nat Neurosci 2013; 16(3): 270-2.
78. Meuret AE, Rosenfield D, Wilhelm FH, et al. Do unexpected panic attacks occur spontaneously? Biol Psychiatry 2011; 70: 985-91.
79. Caldirola D, Bellodi L, Caumo A, Migliarese G, Perna G. Approximate entropy of respiratory patterns in panic disorder. Am J Psychiatry 2004; 161(1): 79-87.
80. Diveky T, Prasko J, Latalova K, et al. Heart rate variability spectral analysis in patients with panic disorder compared with healthy controls. Neuroendocrinol Lett 2012; 33(2): 156-66.
81. Perna G, Dario A, Caldirola D, et al. Panic disorder: the role of the balance system. J Psychiatric Res 2001; 35(5): 279-86.
82. Perna G, Marconi C, Battaglia M, et al. Subclinical impairment of lung airways in patients with panic disorder. Biol Psychiatry 1994; 36(9): 601-5.
83. Lundberg DB, Mueller RA, Breese GR. An evaluation of the mechanism by which serotonergic activation depresses respiration. J Pharmacol Exp Ther 1980; 212: 397-404.
84. Jordan D. Vagal control of the heart: central serotonergic (5-HT) mechanisms. Exper Physiol 2005; 90(2): 175-81.
85. Depuy SD, Kanbar R, Coates MB, Stornetta RL, Guyenet PG. Control of breathing by raphe obscurus serotonergic neurons in mice. J Neurosci 2011; 31(6): 1981-90.
86. de Souza Moreno V, Bicego KC, Szawka RE, Anselmo-Franci JA, Gargaglioni LH. Serotonergic mechanisms on breathing modulation in the rat locus coeruleus. Pflugers Arch 2010; 459(3): 357-68.
87. Halberstadt AL, Balaban CD. Selective anterograde tracing of the individual serotonergic and nonserotonergic components of the dorsal raphe nucleus projection to the vestibular nuclei. Neuroscience 2007; 147(1): 207-23.
88. Kang EH, Lee IS, Park JE, Kim KJ, Yu BH. Platelet serotonin transporter function and heart rate variability in patients with panic disorder. J Kor Med Sci 2010; 25(4): 613-8.
89. Perna G, Alpini D, Caldirola D, et al. Serotonergic modulation of the balance system in panic disorder: an open study. Depr Anxiety 2003; 17(2): 101-6.
90. Yeragani VK, Rao R, Tancer M, Uhde T. Paroxetine decreases respiratory irregularity of linear and nonlinear measures of respiration in patients with panic disorder. A preliminary report. Neuropsychobiology 2004; 49(2): 53-7.
91. Schruers K, Klaassen T, Pols H, et al. Effects of tryptophan depletion on carbon dioxide provoked panic in panic disorder patients. Psychiatry Res 2000; 93(3): 179-87.
92. Schruers K, van Diest R, Overbeek T, Griez E. Acute L-5-hydroxytryptophan administration inhibits carbon dioxide-induced panic in panic disorder patients. Psychiatry Res 2002; 113(3): 237-43.
93. Perna G, Bertani A, Caldirola D, et al. Modulation of hyperreactivity to 35% CO2 after one week of treatment with paroxetine and reboxetine: a double-blind, randomized study. J Clin Psychopharmacol 2004; 24(3): 277-82.
94. Bertani A, Perna G, Migliarese G, et al. Comparison of the treatment with paroxetine and reboxetine in panic disorder: a randomized, single-blind study. Pharmacopsychiatry 2004; 37(5): 206-10.
95. Mobbs D, Marchant JL, Hassabis D, et al. From threat to fear: the neural organization of defensive fear systems in humans. J Neurosci 2009; 29(39): 12236-43.
96. de Oliveira Sergio T, de Bortoli VC, Zangrossi H, Jr. Serotonin-2A receptor regulation of panic-like behavior in the rat dorsal periaqueductal gray matter: the role of GABA. Psychopharmacology 2011; 218(4): 725-32.
97. Jacob CA, Cabral AH, Almeida LP, et al. Chronic imipramine enhances 5-HT(1A) and 5-HT(2) receptors-mediated inhibition of panic-like behavior in the rat dorsal periaqueductal gray. Pharmacol Biochem Behav 2002; 72(4): 761-6.
98. Carr DB, Sheehan DV. Panic anxiety: a new biological model. J Clin Psychiatry 1984; 45(8): 323-30.